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Amazing Tales of Electric Lugworms: Metabolic Physiology Reaches Out

Stephen Palumbi

The Extended Organism: The Physiology of Animal-Built Structures. J. Scott Turner. xii + 235 pp. Harvard University Press, 2000. $47.50.

Tiny silver balls, held and manipulated by insect limbs, shrinking as if by a magician's trick, inexorably disappear. These glittering bubbles are not just ornamental adornments, but spheres of critical life-giving air, an aquatic beetle's lungs in a watery world. How they work is a fascinating story, illustrating how individual organisms can use the external world to fuel their internal metabolism and generate more comfortable homes.

J. Scott Turner uncovers a host of such stories in The Extended Organism: The Physiology of Animal-Built Structures. His thesis is that many of the external structures that organisms build represent the same kind of physiological machinery we typically associate with kidneys, lungs and other squishy bits. He demonstrates his view with verve and enthusiasm in fascinating chapters on how organisms manipulate the external environment to their advantage.

Each story turns on a paradox. In the case of the bubble-carrying beetles, it's that these creatures use their bubbles, which contain ordinary air, to breathe under water; yet given bubbles of pure oxygen to carry, they quickly find themselves suffocating and must return to the surface. Why? Turner tells us in precise detail. In short, the beetle's air-filled bubble acts not as an air tank but as a gill.

A mound of <em>Macrotermes michaelseni</em>Click to Enlarge Image

Turner investigates another paradox when he describes the deposit-feeding lugworms (burrowing marine polychaete worms), which eat marine sediments that are laden with organic material and bacteria. Here the puzzle is that the bacterial content of the sediment is actually higher when it emerges from the tail end of the worm than when it entered the mouth. If worms feed on bacteria in the sediments, why do bacteria prosper in the deep interstices of the worm's gut? Again, we are treated to an intensively detailed description of the external environment, including the strong gradient in oxygen concentration these worms experience in marine sediments. It turns out that the gradient in oxygen, declining to zero in the sulfurous sediments beneath the surface, is an electric gradient as well, and that the worms (and bacteria) use this to advantage in producing metabolic fuel. By harvesting organic matter made without oxygen deep below the surface and combining it with oxygen pumped in from the overlying water, the worms can essentially burn these compounds for fuel, while at the same time providing habitat for growing populations of aerobic bacteria. Every mudflat is a Duracell battery, and the worms have long known it. As Turner explains, "If an animal positions itself in a large-scale gradient in physical potential energy, it can use positive feedback to tap enormous reserves of energy to do its physiological work."

Stories like this form the heart of this book, presenting a novel set of environmental mysteries and revealing their solutions. But Turner does not merely explain the answers?he dissects them and makes us see why they are the answers. Each chapter is, in fact, a hidden lesson in physiology, biomechanics and environmental chemistry. There are long sections that lay the groundwork for the final answers?so long that a hasty reader may become impatient. But each digression pays off in understanding of the basic process explained. By the end of the lugworm section, you understand why oxygen concentrations matter, and how organisms take advantage of this. You understand why bubbles of pure oxygen kill beetles. And you know how termite mounds breathe, how terrestrial earthworms survive outside their aquatic habitat, how crickets shout and how leaf galls grow.

"Physiology is the science of how living things work," asserts Turner, and he adroitly demonstrates his major point, that external physiology can be just as intricate as internal physiology. The examples also raise some intriguing questions about evolution; here, unfortunately, Turner's analysis is less insightful. It is clear that organisms that adjust the environment to their advantage will prosper, but an important distinction is missing in Turner's discussion of the examples he includes. A beetle's air bubble, plucked off the surface and cradled on the lower abdomen, is the property of a single beetle, and any advantages of manipulating the bubble the right way accrue to that one beetle. Any costs are paid by the same beetle too, so in an important sense beetles inherit from their parents their bubble behaviors and the advantages and disadvantages that stem from those behaviors. Thus there is a direct link between selection for a particular bubble behavior and fitness, enough of a direct link that evolution of bubble behaviors could be straightforward. But do all environmental manipulations have such a direct link to evolution?

Consider a second example from the book. The burrowing activities of earthworms increase the soil horizons most conducive to worm health and growth rate. Turner shows in typically detailed fashion exactly how these changes are effected and that this activity represents excellent external physiology. But this situation differs fundamentally from the beetle example: Although worms may inherit the behaviors that generate better soils, the benefits of better soil accrue to all resident worms whether they have the behaviors or not. What if these behaviors are costly? Will selection favor worms that cheat by enjoying these benefits of the altered environment without paying the price?

Overall, the nature of environmental manipulations seems to be important to understanding their evolutionary genesis. Local manipulations that can be controlled by an individual or group seem to be fundamentally different from wholesale regional or global changes that affect all members of a species. Evolutionary explanations as detailed and persuasive as the physiological explanations offered by Turner might allow such distinctions to be more finely understood.

In some measure, such evolutionary distinctions have been explored before?by George C. Williams in his 1966 landmark Adaptation and Natural Selection, by Richard Dawkins in The Extended Phenotype and by John Maynard Smith and Eors Szathmary in The Major Transitions in Evolution. But Turner brings these issues to a head in a final chapter on the evolutionary genesis of extended environmental physiologies, in which he discusses the Gaia hypothesis (that the Earth exhibits "a global physiology, perhaps even a global homeostasis") and how it might account for the physiological nature of environmental changes. Turner is a Gaia advocate, asking whether there is "a global physiology that is mediated by structural modification of the environment." However, this chapter is rather gently written: He recognizes that this is a controversial subject and must be considered as a intellectual challenge.

Nonetheless, I think Turner underemphasizes the evolutionary hurdles a Gaia world must overcome, and how much is known about the nature and height of these hurdles. Turner lays out the main evolutionary problem at the end of the book?that in a world where evolution acts to favor individual advantage, the price of expensive modifications to the environment "for the good of the species" can be avoided by cheaters. How to overcome this cheating tendency is a major hurdle, perhaps one as significant as the taming of individual cells into a multicellular consortium, or the joining of individual genes into a genome. By contrast, environmental modifications for the good of the individual seem commonplace?and the critical question is the extent to which all intricate examples of external physiology, like those so nicely laid out here, can be explained by natural selection on individuals.

The Extended Organism can be read and enjoyed without taking a position on the Gaia question. It is a clever dissection of environmental physiology from a persistent and clever teacher. Like most good teachers, Turner manages to slip a huge range of new information into your head along the way?information that helps change your view of organisms in their world.

I, for one, will never look at a lugworm the same way as before.

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